HIV-1 infection of macrophages dysregulates innate immune responses to Mycobacterium tuberculosis by inhibition of interleukin-10

J Infect Dis. 2014 Apr 1;209(7):1055-65. doi: 10.1093/infdis/jit621. Epub 2013 Nov 21.

Abstract

Human immunodeficiency virus (HIV)-1 and Mycobacterium tuberculosis (M. tuberculosis) both target macrophages, which are key cells in inflammatory responses and their resolution. Therefore, we tested the hypothesis that HIV-1 may modulate macrophage responses to coinfection with M. tuberculosis. HIV-1 caused exaggerated proinflammatory responses to M. tuberculosis that supported enhanced virus replication, and were associated with deficient stimulus-specific induction of anti-inflammatory interleukin (IL)-10 and attenuation of mitogen-activated kinase signaling downstream of Toll-like receptor 2 and dectin-1 stimulation. Our in vitro data were mirrored by lower IL-10 and higher proinflammatory IL-1β in airway samples from HIV-1-infected patients with pulmonary tuberculosis compared with those with non-tuberculous respiratory tract infections. Single-round infection of macrophages with HIV-1 was sufficient to attenuate IL-10 responses, and antiretroviral treatment of replicative virus did not affect this phenotype. We propose that deficient homeostatic IL-10 responses may contribute to the immunopathogenesis of active tuberculosis and propagation of virus infection in HIV-1/M. tuberculosis coinfection.

Keywords: HIV-1; inflammation; interleukin-10; macrophage; tuberculosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • HIV Infections / complications
  • HIV Infections / immunology*
  • HIV-1 / immunology*
  • Host-Pathogen Interactions
  • Humans
  • Immunity, Innate*
  • Immunosuppression Therapy
  • Interleukin-10 / antagonists & inhibitors*
  • Macrophages / immunology*
  • Macrophages / microbiology
  • Macrophages / virology
  • Mycobacterium tuberculosis / immunology*
  • Tuberculosis, Pulmonary / complications
  • Tuberculosis, Pulmonary / immunology*

Substances

  • Interleukin-10